Unique nesting biology of Osmia ( Melanosmia) uncinata, a Palaearctic osmiine bee specialized on thick-barked conifers (Hymenoptera, Megachilidae)

Alpine Entomology 4 2020, 157-171 | DOI 10.3897/alpento.4.53489

> PENSUFT.

7

Alpine
Entomology

Unique nesting biology of Osmia (Melanosmia) uncinata, a
Palaearctic osmuine bee specialized on thick-barked conifers
(Hymenoptera, Megachilidae)

Andreas Miiller’, Rainer Prosi*, Stewart Taylor’, Henning Richter*, Mike Herrmann®, Urs Weibel®

ETH Zurich, Institute of Agricultural Sciences, Biocommunication and Entomology, Schmelzbergstrasse 9/LFO, 8092 Zurich, Switzerland
Lerchenstrasse 81, 74564 Crailsheim, Germany

Firwood, Nethybridge, Inverness-shire, PH25 3DE, United Kingdom

University of Zurich, Vetsuisse Faculty, Clinic for Diagnostic Imaging, Winterthurerstrasse 258c, 8057 Zurich, Switzerland
Sonnentauweg 47, 78467 Konstanz, Germany

Museum zu Allerheiligen, Klosterstrasse 16, 8200 Schaffhausen, Switzerland

NnonF WYN

http://zoobank.org/9 DAC 1 925-5367-4D0F-A877-0582A6FA9928

Corresponding author: Andreas Miller (andreas.mueller@usys.ethz.ch)

Academic editor: Jessica Litman @# Received 21 April 2020 # Accepted 21 June 2020 # Published 30 July 2020

Abstract

Osmia (Melanosmia) uncinata Gerstacker is a Palaearctic megachilid bee distributed from temperate and northern Europe eastwards
to the Russian Far East. The discovery of over 80 nests in Switzerland, southern Germany and Scotland enabled for the first time a
closer investigation of its nesting biology and prompted the assessment of the species’ phenology, distribution and habitat. O. un-
cinata nested in self-excavated burrows inside the bark of both living trunks and dead stumps of Pinus sylvestris. The nests were
excavated at a height of 10-220 cm above ground either on the underside of prominences of longitudinal bark ribs or inside beetle
borings and extended more or less vertically upwards. They consisted of a single straight to slightly curved burrow with rarely one
to three side burrows, had a total length of 1.2-12.0 cm and contained 1-6 brood cells. The brood cells, which faced downwards
with the larval provisions being located in the upper cell half, were separated from each other by one-layered walls of chewed leaves
(“leaf pulp”). The nests were sealed with a plug of 2-4 closely adjacent walls of leaf pulp. DNA metabarcoding of cell and plug walls
revealed that Potentilla and Fragaria (Rosaceae) served as leaf pulp sources. Pre-imaginal mortality amounted to 77%, partly caused
by brood parasites such as Sapyga similis (Sapygidae) and Cacoxenus indagator (Drosophilidae) or predators such as snakeflies (Ra-
phidioptera). At low elevations, O. uncinata needs one year for its development and overwinters as imago inside the nest, whereas in
the subalpine zone of the Alps it has a two-year cycle passing the first winter as prepupa and the second winter as imago. O. uncinata
starts to emerge between the end of March at low elevations and the end of May at higher elevations qualifying as an early flying bee
like the other European O. (Melanosmia) species. The distribution of O. uncinata in Central Europe and Scotland largely coincides
with the occurrence of P. sylvestris. As in the pine, it extends over a wide altitudinal range from below 100 m up to 1900 ma.s.1. and
encompasses dry and wet as well as warm and cold habitats including open pine forests, inner and outer forest edges dominated by
pine and isolated pine groups. At a few locations in the subalpine zone of the Alps, O. uncinata occurs in the absence of P. sylvestris,
here, the thick bark of Larix decidua serves as a substitute nesting substrate.

Key Words

Anthophila, Apiformes, mandibular strength, Osmiini, Rhagium, X-raying

Copyright Andreas Muller et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which
permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

158

Introduction

Osmia uncinata Gerstacker (Megachilidae, Osmiini) is a
Palaearctic mason bee of 8-10 mm body length that is
usually found in or near forests (Figs 1-4). The females
collect pollen mainly on Hippocrepis, Lotus and other
Fabaceae species, although representatives of more than
ten other plant families also serve as pollen hosts (Muller
2018; Westrich 2018). O. uncinata is a member of the
large Holarctic subgenus Melanosmia Schmiedeknecht,
which 1s represented in Europe by 12 mostly cold-adapt-
ed and mountainous species often exhibiting an arctoal-
pine or boreomontane distribution (Rightmyer et al. 2010,
Muller 2020). The females of many O. (Melanosmia)
Species are morphologically very similar and difficult to
identify. Information on the biology of O. (Melanosmia)
species in the older literature should therefore be treated
with caution. In fact, O. (Melanosmia) pilicornis Smith
was formerly assumed to nest in stony ground, in empty
snail shells, under loose bark or in insect burrows in dead
wood until it finally turned out that the species obligatori-
ly gnaws its nests in dead fallen branches of trees (Lem-

Andreas Muller et al.: Nesting biology of Osmia uncinata

oine 2016; Prosi et al. 2016). Similarly, O. (Melanosmia)
nigriventris (Zetterstedt) was repeatedly hypothesized to
nest 1n insect burrows in dead wood, which was found to
be erroneous by a recent study showing that it actually
excavates its nests mainly in pieces of larch and pine bark
lying on the ground (Muller et al. 2019).

Published information on the nesting biology also ex-
ists for O. uncinata, although no nests have ever been de-
scribed in detail. The species was reported to construct its
brood cells in old tree stumps (Friese 1891), in the bark
of pine trees (Bouwman 1922; Stoeckhert 1933; Willems
2010), in burrows of the cerambycid beetle Rhagium in-
quisitor L. (Edwards 2001; Else and Edwards 1996, 2018;
Taylor 2015) or in drilled borings of wooden trap nest
blocks (Westrich in Else and Edwards 2018). However,
the hypothesized use of insect burrows in dead wood as
nesting site raises doubts. First, compared with other rep-
resentatives of O. (Melanosmia) the mandibles of O. un-
cinata females are considerably stronger than those of
species that nest in pre-existing cavities or loose soil but
weaker than those of species that are capable of tunneling
out their nests in hard wood (Miller et al. 2019). Sec-
ond, numerous attempts to establish O. uncinata in trap

Figures 1—4. Osmia uncinata. 1) Female on Lotus corniculatus (Fabaceae). 2) Female on Rubus spec. (Rosaceae; photo A. Jacobs).
3) Male. 4) Female at the entrance of her nest.

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Alpine Entomology 4 2020, 157-171

nests composed of cardboard tubes or drilled borings in
dead wood all have failed (Taylor 2011; Sears et al. 2014;
A. Miller and R. Prosi unpublished). Third, the distribu-
tion of O. uncinata in Central Europe appears to be very
patchy coinciding neither with a certain altitude nor with
overall forest cover. These findings all point to a more
specialized nesting biology than hitherto assumed.

In spring 2019, we discovered in an open pine forest
in eastern Switzerland near Trimmis (Grisons) a strongly
weathered linear burrow on the surface of the bark of a
healthy pine (Pinus sylvestris L.) about one meter above
the ground (similar to Fig. 16). This burrow, which was
3.2 cm long, 5 mm wide and directed vertically upwards,
had undoubtedly been gnawed out by an insect and most
probably run completely inside the bark at the time of its
creation. Indeed, an almost identical burrow was found
in the bark of a neighbouring pine tree, which was en-
tirely hidden and ran several millimeters below the bark
surface. Interestingly, this second burrow contained re-
mains of brood cell partitions built from chewed green
leaves (“leaf pulp”), most probably originating from an
osmiine bee. As O. uncinata was recorded in the same
pine forest, the suspicion arose that these two burrows
could be old nests of this bee species. This suspicion was
later confirmed by the systematic examination of the bark
of numerous P. sy/vestris trees at eight different localities
in Switzerland and southern Germany, which revealed
many old and few new nests, some of which contained
dead or living imagines of O. uncinata.

In the present publication we describe nesting site, nest
architecture and brood parasites of O. uncinata based on
80 nests and compare these Central European nests with
two nests recently found in northern Scotland (Taylor
2015). Furthermore, we identify the nest building materi-
al by DNA analysis of nest closures and brood cell parti-
tions, characterize the phenology and habitat of O. unci-
nata in Central Europe and present a distribution map of
the species’ range.

Methods

Between spring and winter 2019, the bark of Pinus syl-
vestris trees was checked for nests of Osmia uncinata at
seven sites in eastern and northern Switzerland and at one
site in southern Germany, where the species was known
to occur: Sent/Grisons (46°48'45"N, 10°21'36"E; 1100 m
a.s.l.), Versam/Grisons (46°48'28"N, 9°20'03"E; 650 m
a.s.1.), Trimmis/Grisons (46°53'23"N, 9°33'50"E; 750 m
a.s.l.), Lommis/Thurgau (47°31'32"N, 8°58'51"E; 550 m
a.s.l.), Hutntwangen/Zurich (47°35'21"N, 8°30'55"E;
400 m as.l.), Beringen/Schaffhausen (47°42'03"N,
8°35'37"E; 550 m as.l.), Merishausen/Schaffhausen
(47°46'22"N, 8°36'42"E; 650 m a.s.l.) and Immending-
en/Baden-Wuerttemberg (47°55'56"N, 8°41'39"E; 700 m
a.s.l.). At each site, both trunks and stumps of P. sy/vestris
were systematically examined from the ground up to a
height of about 2.25 m with the aid of a torch and a pocket

159

mirror, which facilitated the discovery of nest entranc-
es hidden in bark cracks, fissures or ruptures. Bark areas
containing potential nests as suggested by open circular
holes of 4-5 mm in diameter, by nest plugs built from
leaf pulp or by more or less exposed vertical burrows of
4—5 mm width were cut out and transported back to the
lab. Old nests were directly dissected with a pocket knife,
whereas new nests sealed with a nest plug were X-rayed
first at the Vetsuisse Faculty of the University of Zurich
using both a Bucky Diagnost CS/TH X-Ray (Philips)
combined with a Profect CS Mammo-Reader (Fujifilm)
and an ultra-high resolution digital radiography system
(UltraFocus 100, Faxitron), before they were opened. In
addition, a piece of bark from a burnt Pinus sylvestris
stump in northern Scotland near Aviemore (57°11'43"N,
3°49'26"W; 220 m a.s.l.), which contained two nests of
O. uncinata built within beetle borings of Rhagium in-
quisitor (Cerambycidae), was X-rayed. These nests were
discovered by Gus Jones and described by Taylor (2015).
In April 2020, the bark of trunks and stumps of Larix de-
cidua Miller in a subalpine larch forest near Blatten in
the Lotschental/Valais (46°25'20"N, 7°49'00"E; 1600—
1800 m a.s.l.) was examined for nests in close vicinity of
recent O. uncinata sightings.

To identify the source of the nest building material used
by O. uncinata, DNA metabarcoding of nest plugs and
brood cell walls consisting of leaf pulp was performed
by Eurofins Medigenomix GmbH (Ebersberg, Germany).
The leaf pulp material used for DNA analysis originated
from two nests discovered in Lommis (2 cell walls) and
Immendingen (3 plug and 3 cell walls). DNA of each of
the two samples was extracted with the Maxwell 16 FFS
nucleic acid extraction kit (Promega) following the man-
ufacturer’s manual. From the extracted DNA, barcoding
sequences of the nuclear marker ITS2 and the chloroplast
marker trnL were PCR amplified using target specific
next-generation sequencing primers and analysed by am-
plicon sequencing on the Illumina MiSeq platform. The
amplified sequences were sorted into sequence clusters
according to their similarity, each represented by a master
sequence. The master sequences were identified to spe-
cies or genus level by comparing them with known plant
sequences made available by the NCBI database.

To clarify the phenology and distribution of O. unci-
nata, we conducted a comprehensive literature survey,
gathered unpublished records from public and private
entomological collections and retrieved distributional
data from several public databases (for details see Ac-
knowledgments and Suppl. material 1, which contains a
complete list of all distributional data). For the phenol-
ogy, only records from Central Europe (Austria, Czech
Republic, French Alps, Germany, Italian Alps, Liechten-
stein, Poland, Slovakia, Slovenian Alps and Switzerland)
were considered.

To examine whether the distribution of O. uncinata 1s
confined to stands of P. sy/vestris, we applied three meth-
ods. First, we compared the Swiss records of O. uncinata
(n = 198) with those of P. sy/vestris using the open-source

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160

geographic information system QGIS, version 3.4 (www.
qgis.org). These records were made available by the Cen-
tre Suisse de Cartographie de la Faune (CSCF) for O. un-
cinata and the Swiss National Forest Inventory carried
out by the Swiss Federal Institute for Forest, Snow and
Landscape Research (WSL) for P. sylvestris (WSL 2019).
Second, we checked each square kilometre of the Swis-
stopo grid (www.swisstopo.admin.ch), for which records
of O. uncinata were known (n = 172), for the presence
of P. sylvestris stands (“pine presence”) by the follow-
ing step-wise procedure: 1) analysis of aerial photos pro-
vided by the Swiss mapping platform (https://map.geo.
admin.ch); if the occurrence of P. sylvestris stands was
uncertain after the aerial photo analysis, 11) we contact-
ed the appropriate bee recorder or forest official; if the
presence of P. sylvestris stands was still unclear, 111) we
checked the square kilometre in the field. Pine presence
was differently defined depending on the precision of the
bee record: if the record was precise to the nearest 250 m,
pine presence was assumed when there were pine stands
in a radius of 250 m around the record; if the record was
less precise, pine presence was assumed when there were
pine stands within the square kilometre. Third, we made
a survey among German and Austrian bee experts asking
them to judge the presence of P. sy/vestris stands 1n a radi-
us of 250 m around each of their own O. uncinata records
according to the following three categories: 1) presence of
P. sylvestris stands certain or highly probable, 11) absence
of P. sylvestris stands certain or highly probable, 111) pres-
ence of P. sylvestris stands unclear.

Results
Nesting biology

Nesting site

Nests of Osmia uncinata were found at each of the eight
study sites. In total, 80 nests were discovered, 71 of which
were abandoned and one to several years old, whereas
nine were new containing living or freshly dead progeny
(n = 8) or an adult female, which had died within her first
unfinished brood cell for unknown reasons (n = 1). All
nests were built inside the outermost bark layer of trunks
of living and healthy trees of Pinus sylvestris, which
grew at sunny places of open pine stands (Figs 5-10).
The trunk diameter at breast height of trees selected as
nesting sites varied from 16—76 cm (Fig. 15a). All nest
entrances, which were circular in shape and had a diam-
eter of 4.25-4.75 mm, were located below 1-3 cm thick
prominences of longitudinal bark ribs and were visible
only from below (Figs 4, 11-14, 17). The only exception
was a single nest that entered the bark on the lateral side
of arib. The nest entrances were at a height of 16-220 cm
above the ground (Fig. 15b). As the bark of pine trunks
usually becomes considerably thinner at heights between
two and three metres offering increasingly less suitable

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Andreas Muller et al.: Nesting biology of Osmia uncinata

nesting sites, the proportion of overlooked nests higher
than two metres above the ground is expected to be low.
The bark areas containing nests were exposed in all direc-
tions (Fig. 15c). However, most of the nests were located
on the east, southeast, south and southwest side of the
trunks, whereas a much smaller proportion was on the
less sun-exposed trunk areas.

The nesting site described above corresponds to the
behaviour of three females of O. uncinata, which ex-
amined the bark of Pinus sylvestris while searching for
a suitable nesting place near Trimmis on 8.6.2019. One
female checked the bark of a dead pine stump, while the
others patrolled the bark of living pine trunks. The latter
two females started their search at the base of the tree
and flew slowly along the sunny side of the trunk up to a
height of 1.5—2.5 m, before they left and flew to the base
of a neighbouring pine tree to start a new upwardly search
flight. All three females repeatedly interrupted their flight
and landed on the bark to carefully inspect fissures, frac-
tures and prominences. The same behaviour was ob-
served in two females of the sapygid wasp Sapyga similis
(Fabricius), which examined the pine bark most probably
in search for nests of their host O. uncinata (see below).
Host-nest searching females of S. similis at the bark of
old pine trees were also reported by Tischendorf (2002).

Three nests containing living progeny or freshly dead
adults at the time of their discovery were most likely re-
used as indicated by the presence of at least one year old
remains of leaf pulp walls. Whether such nests were en-
larged in the year of reuse by prolonging the main burrow
or by excavating side burrows is unclear. Other aculeate
Hymenoptera also used the abandoned nesting burrows
of O. uncinata to place their brood cells, such as Heria-
des, e.g. H. truncorum L. (Megachilidae, n= 1), Hylaeus,
e.g. H. communis Nylander (Colletidae, n = 11), Passa-
loecus, e.g. P. eremita Kohl (Crabronidae, n = 2), 7ryp-
oxylon (Crabronidae, n = 1), Deuteragenia (Pompilidae,
n=2) and eumenine wasps (Vespidae, n = 1); in five other
reused nests with remains of earthen cell walls the owner
could not be identified.

Nest architecture

The nests were all tunneled out by the females of Osmia
uncinata with no indication that pre-existing burrows
e.g. of cerambycid beetle larvae were used. The nesting
burrows were carefully carved out and measured most-
ly 4.25-4.75 mm in diameter (range 4.0-5.75 mm). They
were neither lined with glandular secretions nor with leaf
pulp except sometimes for small areas of a few square
millimetres covered with a thin layer of leaf pulp, which
was probably applied to smooth out irregularities or to fill
small cracks. The burrows, which were completely hidden
2—13 mm below the bark surface, ran more or less vertically
upwards and parallel to the trunk surface (Figs 16, 18—25).

The nests usually consisted of a single straight to
slightly curved burrow of 1.3—8.0 cm length (n = 63;
Figs 15d, 16, 18-22). In eight nests, however, one (n= 5),

Alpine Entomology 4 2020, 157-171

Figures 5—14. Nesting site of Osmia uncinata. 5-10) Position of nests in the bark of Pinus sylvestris trunks. 11-14) Nest entrances
below prominences of longitudinal bark ribs.

two (n = 2) or three (n = 1) side burrows branched off the
main burrow (Figs 23—25). These side burrows were ex-
cavated in the same plane as the main burrow and the lon-
ger ones ran parallel to the main burrow. The total length
of nests with a main burrow and one to three side burrows
varied from 4.7—12.0 cm (Fig. 15d).

The new nests as well as those old nests, for which the
number of brood cells could properly be ascertained due

to remains of cell partitions or dead bee progeny, con-
tained 1-6 brood cells (Fig. 15e). The brood cells were
constructed either singly in short burrows or in a linear
series of 2—5 in longer burrows (Figs 28-30). They had a
length of 7.5—11 mm including the outer cell partition, a
width of 4.5—5.75 mm and were slightly broadened in the
middle (n = 49). Given these brood cell dimensions, some
old nests with a total burrow length exceeding 7-8 cm

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162
20 - a) Trunk diameter (n=64) 20
15 15
10 10
5 5
0 0
oe a ~ xe Ae oe a Ri a
20 - c) Nest exposure (n=74) 8
15 6
10 4
5 2
0 0

N NE E SE S SW W NW
20 + d) Nest length (n=71)

15
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a ae or Sa © ° © aN aa Rr

Andreas Muller et al.: Nesting biology of Osmia uncinata

b) Nest height (n=75)

e) Brood cell number (n=17)

1 old nests
HB new nests

Figure 15. Nest parameters of Osmia uncinata. a) Trunk diameter at breast height of Pinus sylvestris trees selected as nesting site.
b) Height of nest entrance above the ground. c) Exposure of nest. d) Length of nesting burrow. e) Number of brood cells. Grey =

abandoned nests; blue = nests occupied upon discovery.

might possibly have contained more than six brood cells.
In spite of the vertical orientation of the nesting burrows,
the larval provisions were located in the basal, 1.e. upper
half of the brood cell (Figs 29, 30).

Each brood cell was sealed towards the nest entrance
with a one-layered wall built from leaf pulp without addi-
tion of other material (Figs 28-30). These cell walls had
a maximum marginal width of 1-2 mm and a minimum
central width of 0.25—0.75 mm (n= 13). As revealed by a
threshold of leaf pulp at the entrance of a still empty brood
cell, the females mark the position of the later cell wall
before they begin to provision the cell; this threshold was
ring-shaped, which seems to be typical for Osmia species
of the subgenus Me/anosmia (Miller et al. 2019). Between
the outermost cell wall and the innermost wall of the nest
plug was an empty vestibule, which ranged in length from
2.75—11 mm (n= 7); in one exceptional case the vestibule
was 22 mm long (Fig. 30). The nest plug, which measured
4—9 mm in total length (n = 8), consisted of two (n = 2),
three (n = 5) or four (n = 1) one-layered walls made from
leaf pulp (Figs 26—28, 30). These plug walls were con-
structed immediately behind each other, rarely enclosing
a few loose clumps of leaf pulp between them. They were

alpineentomology.pensoft.net

thicker than the cell walls and had a maximum margin-
al width of 1.5—3.5 mm and a minimum central width of
0.5—1.25 mm (n= 23). The outermost plug wall was either
flush with the nest opening (n = 3) or slightly recessed by
1—3 mm (n = 3); in two reused nests, it was at a distance
of 1.0 cm and 2.1 cm from the opening.

DNA metabarcoding revealed that the brood cell and
plug walls of two nests were constructed from masticated
leaves of Fragaria spec. and Potentilla spec. (both Ro-
saceae) (Tab. 1). In addition, very low proportions of se-
quence reads corresponded to Asteraceae and Viola (Vi-
olaceae). Although the percentage of reads obtained by

Table 1. Origin of the masticated green leaves used by Osmia
uncinata to build the walls of brood cells and nest plugs based on
DNA metabarcoding of a sample of eight walls of two nests orig-
inating from two localities in Switzerland and southern Germany.

Locality Plant taxon % sequence
reads
Lommis/Thurgau (1 nest, 2 walls) Fragaria spec. 100
Immendingen/Baden-Wuerttemberg — Fragaria spec. 77.2
(1 nest, 6 walls) Potentilla spec. 17.6
Asteraceae spec. 22h
Viola spec. 25

Alpine Entomology 4 2020, 157-171

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163

fo

Figures 16—25. Nest architecture of Osmia uncinata. 16) Several years old nest after uppermost bark layer has flaked off. 17) En-
trance to old nest seen from below. 18-25) Dissected nests consisting of a single burrow (18-22) or of one to three side burrows

branching off the main burrow (23-25).

next-generation sequencing is only a rough indication for
the relative amount of a plant taxon in the extracted DNA,
this low proportions might be due to contaminations.

Larval mortality
Osmia uncinata successfully developed to the imaginal

stage only in two of the eight nests that were occupied
upon discovery: a three-celled nest produced one male

and a six-celled nest produced four females and one male
(Fig. 30). In five brood cells of four nests, two females
and three males of the sapygid wasp Sapyga similis
(Fabricius) developed. Three adjacent cells within the
same nest were destroyed by the drosophilid fly Cacox-
enus indagator Loew. The content of two neighbouring
cells within the same nest was devoured by the larva of
a snakefly (Raphidioptera). And in ten cells distributed
among four nests the larvae of O. uncinata died for un-

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164 Andreas Muller et al.: Nesting biology of Osmia uncinata

Figures 26-30. Nests of Osmia uncinata. 26-27) Nest entrances sealed with leaf pulp. 28) Dissected nest with three brood cells each con-
taining a cocoon. 29) Dissected unfinished nest with cocoon in uppermost cell and dead larva on food provision in two cells. 30) X-rayed
nest with six cells containing four overwintering females, one overwintering male (outermost cell) and a dead larva on food provision.

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Alpine Entomology 4 2020, 157-171

known reasons. In summary, a successful development
of O. uncinata failed in 20 out of 26 brood cells, which
corresponds to a pre-imaginal mortality of 77%.

The Scottish nests

The two nests of Osmia uncinata discovered in the Scot-
tish Highlands were located inside the bark of a Pinus
sylvestris stump (Fig. 31). They were constructed by the
same female, which entered each nest by an exit hole of
the xylophagous beetle species Rhagium inquisitor L.
(Cerambycidae). The two exit holes lay 10 cm and 11 cm
above the ground and were separated by a distance of
less than 5 cm (Figs 31, 32). Upon discovery, one nest
had been sealed by the female bee with leaf pulp (nest

165

1), whereas the other was being provisioned (nest 2).
Each nest consisted of a 4.5—5 mm wide burrow, which
had a length of 1.2 cm in nest 1 and 4.0 cm in nest 2
(Figs 33, 34). The two nesting burrows were tunneled
out by the female at the roof (nest 1) or the upper lateral
corner (nest 2) of the beetle boring. Both were directed
upwards and they contained one (nest 1) and three (nest
2) brood cells. The presence of numerous small borings
of anobiid beetles — probably Ernobius mollis (L.) — in
the bark directly above the Rhagium exit areas was likely
the reason why the short nesting burrow of nest 1 was not
advanced further upwards and why the burrow of nest 2
was started laterally rather than apically within the beetle
boring (Figs 33, 34). Nest 1 was sealed with walls of leaf
pulp both at the entrance of the short nesting burrow and

Figures 31-34. Scottish nests of Osmia uncinata. 31) Stump of a burnt Pinus sylvestris tree containing two nests. 32) Female of
O. uncinata on bark with three large exit holes of Rhagium inquisitor, of which the upper two served as entrance to one nest each:
nest | (left) is sealed, nest 2 (upper right) is being provisioned; note the bark particles that have accumulated below nest 2, indicating
the former digging activity of the female. 33, 34) X-rayed bark (left) and dissected nests (right) with nest 1 excavated at the roof and
nest 2 excavated at the upper lateral corner of the Rhagium boring; the large dark spots on 33) are the three Rhagium exit holes, the
numerous small spots are exit holes of anobiid beetles. The red arrows indicate the entrance to the excavated nesting burrows and
the red frames the enlarged section on the opposite image.

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166

at the opening of the Rhagium boring at the bark surface.
Nest 2 remained unsealed, probably because the female
died before the last brood cell was finalized.

Nests in the Létschental/Valais

In the subalpine larch forest searched for nests of Osmia
uncinata, three abandoned nests and one new nest were
discovered in the bark of living trees of Larix decidua,
which grew at an altitude between 1630-1780 ma.s.l. and
measured 61—79 cm in trunk diameter. The nest entrances
were 77—146 cm above the ground and — as in the nests in
pine bark — were situated below prominences of longitu-
dinal bark ribs. The four nests were located on the south
(n = 2) and southeast (n = 2) side of the trunks. Their
architecture exactly corresponded to that of the nests in
pine bark described above. The new nest contained two
brood cells with an overwintering prepupa each of Sapy-
ga spec. and O. uncinata.

Phenology and overwintering stage

In Central Europe, the imaginal period of Osmia uncinata
varies depending on the altitude (Fig. 35, Suppl. mate-
rial 1). At the lowest elevations below 500 m a.s.I., the
flight activity may start already at the end of March and

Elevation
2000
1900
1800
1700
1600 @
1500 @

1400 ©
1300 ©

1200 Ne
1100

1000

900

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700 @ )
600

500

© male (n=92) © female (n=336)
number of records C >3 O 3 O2 o1

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Andreas Muller et al.: Nesting biology of Osmia uncinata

rarely extends beyond the end of June, whereas at eleva-
tions above 1500 maz.s.]. in the subalpine zone of the Alps
the imagines usually do not emerge before mid June and
normally fly till the end of July.

Six brood cells originating from two nests built in 2019
at an altitude of 550 m and 700 m a.s.l. contained living
adults when they were opened in fall (Fig. 30), indicating
that O. uncinata has a one-year cycle at lower elevations
and overwinters as fully developed imago within the nest.
In contrast, a brood cell in a nest built in 2019 at an alti-
tude of 1630 m a.s.I contained a prepupa of O. uncinata
in April 2020, suggesting that O. uncinata passes at least
its first winter in the prepupal stage in the subalpine zone
of the Alps (see Discussion).

Distribution and habitat

Osmia uncinata has a vast distribution occurring from
temperate and northern Europe eastwards to the Rus-
sian Far East (Fig. 36). It inhabits a wide belt between
43° and 70° northern latitude, extending from 5° western
to 153° eastern longitude. It is distributed from sea level
up to about 1900 m a.s.l., with most records above 1500
m a.s.l. being situated in the inner alpine valleys of the
Valais, Grisons and South Tyrol. It has been recorded
from western Europe (Scotland, Belgium, Netherlands,

oN, Oo o> Sa S-Ni ho OO 548. th
SR ee Se cag ee ee eee Ses
Oooo oO OC COCclUCUCUrOCUCUCW Cc OCC OO CO Oo
SUMPTER Severe Eee aeMM era
—s —_—
A2HRSsRS HAS GHSASHES
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wow FR BR PKR BR BR OOTY oa oO

Oo oOo fF Se NHN NH CO OC H|H | NN COCO DO = =| PN
SGB>GOLSBSBGRS2FRSG5SBSERUS
oo oo0odoeoooo Toc ooc9aqncoo9o:9o
PPP PPANAAWDANAATN S SP SO
Or-> fF NY NY WO ODO fSBeerN NM WwW OC | FN PD
ASASHRSHRSASAAHASAS SG
oo ocoomcmlclcCWmUCCOUCcOUCcOOUCcOOUCcUCOlOlcUCOCOUCcOOUCcUOoOlUmcUC Cc OWUCcOUCcUODUCOD
DODD D DOAN NNN NN OO CO OO CO

Five days period

Figure 35. Phenology of Osmia uncinata in Central Europe. For each period of five days, the number of female and male records
per elevation is given. For a given locality and date, only one record per sex was considered.

alpineentomology.pensoft.net

Alpine Entomology 4 2020, 157-171 167

‘ f ae ot ¢ Z : is ae 3 Pos
Figure 36. Distribution of Osmia uncinata. See Suppl. material 1 for a complete list of all distributional data. Made with Natural
Earth (www.naturalearthdata.com).

Figure 37. Swiss records of Osmia uncinata (n = 198) mapped onto the distribution of Pinus sylvestris in Switzerland. Grey = sample
plots of the Swiss National Forest Inventory (NF) without occurrence of P. sylvestris; red = sample plots of the NFI with occurrence
of P. sylvestris; green = records of O. uncinata with pine presence; blue = records of O. uncinata without pine presence; black = re-
cords of O. uncinata not assignable to a square kilometre. Data made available by the Centre Suisse de Cartographie de la Faune
(CSCF) for O. uncinata and the Swiss Federal Institute for Forest, Snow and Landscape Research (WSL) for P. sylvestris (WSL 2019).

Luxembourg, northern and southeastern France), cen-
tral Europe (Switzerland, Liechtenstein, Germany,
northern Italy, Slovenia, Austria, Czech Republic, Slo-
vakia, Poland), northern Europe (Denmark, Norway,
Sweden, Finland, Lithuania, Latvia, Estonia), eastern
Europe (northern Ukraine, central and northern Europe-

an Russia) and Asian Russia (Western Siberia, Eastern
Siberia, Far East).

Mapping of the 198 Swiss records of O. uncinata onto
the distribution of Pinus sylvestris in Switzerland re-
vealed a distinct match between the occurrence of the bee
species and the presence of pine stands (Fig. 37). Excep-

alpineentomology.pensoft.net

168

tions were few regions in the Valais (L6tschental, Ober-
goms), Bernese Oberland (Gadmental) and the Grisons
(Val Mustair), where O. uncinata was recorded despite
the lack of P. sylvestris. Out of the 198 Swiss O. uncinata
records, 26 could not be assigned to a square kilometre
and were excluded from the analysis of pine presence
(see Methods). Among the remaining 172 records, pine
presence was confirmed for 167 records (97.1%) and ex-
cluded for five records (2.9%). These five records orig-
inated from the Lotschental (Valais; n = 2), Obergoms
(Valais; n= 1), Gadmental (Berne; n= 1) and Val Mustair
(Grisons; n = 1) and were situated at elevations between
1500 and 1900 m a.s.l.. The identification of the bee in-
dividuals collected at these five localities proved to be
correct with the exception of the Bernese record, which
could not be confirmed as the specimen was not avail-
able. The presence of P. sy/vestris in a radius of 250 m
around the 70 records of O. uncinata reported by German
and Austrian bee experts was certain or highly probable
for 56 records (80.0%), highly improbable for one record
(1.4%) and unclear for 13 records (18.6%).

Discussion
Nesting biology

Osmia uncinata nests in self-excavated short burrows
in the outermost bark layer of Pinus sylvestris trees up
to slightly more than two metres above the ground. Al-
though all Central European nests were found in the bark
of trunks of living trees, the observation of a female that
examined the bark of a stump while searching for a suit-
able nesting site indicates that nests can also be tunneled
out in the bark of stumps or dead trunks. In fact, the two
nests of O. uncinata from Scotland were dug out in the
bark of a burnt stump and Stoeckhert (1933) mentions
pine stumps as nesting sites of O. uncinata. Based on the
latter author, pieces of pine bark lying on the ground are
occasionally also colonized. However, as O. nigriventris
was found to occur at the very same locality, the nest
mentioned by Stoeckhert most probably belonged to
the latter species, which typically nests in detached bark
pieces (Miller et al. 2019).

O. uncinata is one of the few osmiine bee species
known to excavate its nests 1n wooden substrate. Among
the Osmiini, such a behaviour appears to be restricted
to Osmia species of the subgenus Me/anosmia (Pro-
si et al. 2016). It only has been recorded so far in the
Palaearctic O. nigriventris and O. pilicornis and in the
Nearctic O. bucephala Cresson (Packard 1868; Prosi et
al. 2016; Miller et al. 2019). The mandibles of O. un-
cinata females are considerably stronger than those of
related Palaearctic O. (Melanosmia) species nesting in
pre-existing cavities or loose soil, but distinctly weaker
than those of O. nigriventris and O. pilicornis breeding
in self-excavated burrows (Muller et al. 2019). The lat-
ter two species often excavate their nests in hard wood,
which requires stronger mandibles than for tunneling out

alpineentomology.pensoft.net

Andreas Muller et al.: Nesting biology of Osmia uncinata

nests in relatively soft bark. Thus, the female mandibles
of O. uncinata appear to be well adapted for gnawing in
bark but are probably not strong enough to excavate nests
in hard wood, supporting the assumption that O. uncinata
is strictly specialized to bark for nesting.

The nesting burrows of O. uncinata were invariably
oriented vertically upwards with the nest entrance situated
at the lower end. Such an orientation is expected to be ad-
vantageous as rain runoff descending along the bark sur-
face cannot enter the nest. Interestingly, O. uncinata posi-
tions its larval provisions in the upper half of the brood cell
resulting in cells that face downwards. Downward-facing
brood cells are known only in very few bee species (Dan-
forth et al. 2019), e.g. in the Neotropic Hy/aeus tricolor
(Schrottky) (Colletidae), in the Palaearctic Anthidiellum
strigatum (Panzer) (Megachilidae) and occasionally also
in the Palaearctic Heriades truncorum (L.) (Megachili-
dae) (Sakagami and Zucchi 1978; Le Goff 2003; Westrich
2018). Why the provisions of these species do not run out
of the brood cell during and after provisioning is unclear,
but might be due to a combination of surface tension and
viscosity (Danforth et al. 2019). As a consequence of the
upper position of the provisions, the larvae are forced to
feed in a hanging, upside down position making them sus-
ceptible to fall down to the cell bottom, from where they
are hardly capable of reaching the provisions again.

Masticated green leaves of the two closely related
genera Fragaria and Potentilla (Rosaceae) served as
nest building material for O. uncinata. Both genera are
also exploited by other O. (Melanosmia) species as leaf
pulp sources, such as O. (Melanosmia) nigriventris and
O. (Melanosmia) pilicornis (Prosi et al. 2016; Muller
et al. 2019). This finding suggests that the selection of
leaves for manufacturing leaf pulp might be far from ac-
cidental. In fact, several osmiine bee species belonging
to the genus Hoplitis and to Osmia subgenera other than
Melanosmia were also recorded to harvest leaf pulp from
rosaceous genera, such as Alchemilla, Fragaria, Potentil-
la, Rosa and/or Sanguisorba (Miller and Richter 2018),
supporting the view that the leaves of Rosaceae species
might possess particularly favourable properties as nest
building material. However, O. uncinata does not seem
to be strictly specialized to Rosaceae for harvesting leaf
pulp since a female was observed in the Netherlands bit-
ing off leaf material from Betula pendula Roth (Betulace-
ae) (Willems 2010).

The nests of O. uncinata discovered in the course of
the present study rarely contained more than four brood
cells, which 1s in line with Scottish nests found to contain
one to three cells (Else and Edwards 2018, this study).
As the females of osmiine bees usually lay from ten to
20 eggs during their lifetime under natural conditions
(Raw 1972; Hawkins 1975; Correia 1981; Haeseler 1982;
Miller 1994; Danforth et al. 2019), the females of O. un-
cinata are expected to build two or more nests during
their flight period. The construction of few-celled nests
might be a strategy to reduce the risk to lose all proge-
ny after a brood parasite has detected a nest. In fact, the
pre-imaginal mortality in 26 brood cells of eight nests of

Alpine Entomology 4 2020, 157-171

O. uncinata amounted to 77%, which is unusually high
for solitary bees (Minckley and Danforth 2019, but see
Prosi et al. 2016 and Ivanov and Fateryga 2018). The high
pressure exerted by brood parasites may not only explain
the low number of brood cells per nest, but also why
O. uncinata usually occurs in very low densities even at
localities where there are many host flowers and numer-
ous suitable nesting sites.

Contrary to the literature (Else and Edwards 1996,
2018; Edwards 2001), the Scottish females of O. uncinata
do not place their brood cells in pre-existing beetle borings
of Rhagium inquisitor. Instead, they use the Rhagium exit
holes only to enter the bark before they excavate their own
nest inside the bark. Thus, the only difference between the
Central European and the Scottish nests of O. uncinata
is that nest excavation started below bark prominences in
the former and inside Rhagium borings in the latter. This
difference is unlikely to be geographical but might rather
be related to the thickness of the bark. We hypothesize
that Central European females occasionally also enter the
bark through exit holes of xylophagous beetles particular-
ly when the bark lacks strong longitudinal ribs with trans-
versal cracks, and that Scottish females sometimes also
use the underside of bark prominences as starting point
for excavating nests in case that the bark is thick enough.

Phenology and overwintering stage

Like other European representatives of the subgenus Mel-
anosmia, which are early flying bees active in spring and
early summer (Prosi et al. 2016; Westrich 2018; Miller
et al. 2019), Osmia uncinata emerges in phenological
spring, 1.e. between the end of March at low altitudes and
the end of May at higher altitudes. The overwintering of
O. uncinata in the imaginal stage as found in the present
study for elevations below 800 m a.s.l. is in line with this
early flight period. In contrast to its one-year cycle at low-
er elevations, O. uncinata appears to need two years for
its development in the subalpine zone of the Alps, where
a nest at 1630 m a.s.l. still contained a prepupa in April.
As the time span between the end of winter and the onset
of the early flight period is hardly long enough at this
altitude to allow for the metamorphosis to the imaginal
stage, we hypothesize that O. uncinata passes the first
winter as prepupa and the second winter as diapausing
adult at higher elevations. Such an astonishing flexibili-
ty in adapting the duration of development depending on
climatic conditions is also known from other osmiine bee
species (Forrest et al. 2019).

Distribution and habitat

The range of Osmia uncinata in Central Europe largely
coincides with the occurrence of Pinus sylvestris as re-
vealed by the finding that pine presence was judged to be
highly improbable for only a tiny fraction of the Swiss,
German and Austrian O. uncinata records. The bee’s dis-

169

tribution extends over a wide altitudinal range from below
100 m up to 1900 m a.s.l. and encompasses both dry and
wet as well as both warm and cold habitats correspond-
ing well to the distribution of P. sy/vestris, which is char-
acterized by a very wide ecological amplitude (Brandli
1998; Houston et al. 2016). This coincidence between the
occurrence of O. uncinata and P. sylvestris 1s not restrict-
ed to Central Europe. It also applies to Scotland, where
O. uncinata is closely associated with remnants of the
ancient Caledonian Forest dominated by P. sylvestris and
older pine plantations (Falks and Lewington 2015; Else
and Edwards 2018), and probably even to the entire range
of O. uncinata. In fact, almost all known records of O. un-
cinata fall neatly into the distribution of P. sylvestris as
given by Caudullo et al. (2017). Possibly for climatic rea-
sons, however, O. uncinata 1s absent from several south-
ern regions, where relictual stands of P. sy/vestris occur,
such as northern Iberia, southeastern Europe, the Crimea,
northern Turkey and the Caucasus. Interestingly, numer-
ous records of O. uncinata in northwestern Germany, the
Netherlands, Belgium and northern France lie outside the
native range of P. sylvestris (Caudullo et al. 2017), sug-
gesting a rather recent colonization after the widespread
introduction and naturalization of this pine species all
over western Europe during the last few centuries.

At higher altitudes above 1500 m as.l. in the subal-
pine zone of the Swiss Alps (Lotschental, Obergoms, Val
Mustair) there exist a few reliable records of O. uncina-
ta at localities where P. sylvestris does not occur. Dom-
inant tree species at these localities are Picea abies (L.)
Karsten, Pinus cembra L., Pinus mugo Turra and/or Larix
decidua. Since the former three conifers have only a thin
bark, they are unsuitable as nesting site for O. uncina-
ta. In contrast, the bark of L. decidua is similar to that
of P. sylvestris in both thickness and consistency. There-
fore, we strongly assume that O. uncinata uses the bark
of L. decidua as a substitute nesting substrate particular-
ly at elevations above 1400 m a.s.l., where P. sylvestris
becomes rare and L. decidua common (Brandli 1998).
This assumption is supported by the discovery of several
O.uncinata nests in Larix bark at 1630-1780 m a.s.l. in
the Lotschental/Valais.

The pronounced preference of O. uncinata for thick-
barked P. sylvestris trees appears to be the main factor de-
termining the bee’s habitat in Central Europe. Pines that
are well exposed to sun and weather form particularly thick
bark (A. Rigling, personal communication) possibly ex-
plaining why O. uncinata mainly occurs in open pine for-
ests, along outer and inner forest edges dominated by pine
or around isolated pine groups without any obvious clear
preference for altitude, humidity or thermal conditions.

Conclusions

Osmia uncinata shows a patchy distribution in Central Eu-
rope due to its specialization to Pinus sylvestris stands, it
usually occurs only in low population densities rendering it

susceptible to local extinction, and it is red-listed in Switzer-

alpineentomology.pensoft.net

170

land, several German states and in Great Britain (Falk 1991;
Amiet 1996; Scheuchl and Schwenninger 2015), which all
call for measures to preserve and promote populations of
this rare bee. The most promising measures are 1) to aug-
ment the supply of suitable nesting sites by thinning pine
stands to expose individual trees to direct sunlight or by lib-
erating free-standing pines from adjacent shadowing shrubs
or overhanging branches, and 11) to ensure a sufficient quan-
tity of suitable pollen host plants in the vicinity of potential
nesting sites, above all Lotus and Hippocrepis (Fabaceae).

Acknowledgements

F. Amiet, G. Artmann, M. Aubert, M. Blosch, P. Bogusch,
M. Bur, F. Burger, R. Burger, A.W. Ebmer, J. Esser, H.-J.
Fligel, U. Frommer, D. Genoud, G. Le Goff, A. Gogala,
P. Heller, A. Herb, K. Hirt, S. Hopfenmiller, M. Klemm,
W.-H. Liebig, K. Mandery, K. Mehdi, R. Neumeyer, T.
Peeters, C. Praz, M. Proshchalykin, P. Rasmont, C. Ras-
mussen, G. Reder, M. Reemer, K. Rennwald, A. Rey, E.
Scheuchl, K.-H. Schmalz, C. Schmid-Egger, H. Schwen-
ninger, C. Sedivy, J. Smit, A. Stellmacher, J. Straka, R.
Theunert, H. Tinner, S. Tischendorf, J. van der Smissen,
J. Voith, R. Wenger and H. Wiesbauer provided distribu-
tional data of Osmia uncinata and/or judged the presence
of Pinus sylvestris around their own O. uncinata records.
U.-B. Brandli, A. Baltensweiler and F. Cioldi made Swiss
distributional data of P. sylvestris from the Swiss Na-
tional Forest Inventory available. F. Bott, S. Cathomen,
R. Caviezel, A. Egger, R. Gschwend, R. Helfenberger,
J. Heuberger, B. Huber, F. Isler, C. Riatsch, D. Rohrer,
P. Rovina and T. Studer informed about the presence of
P. sylvestris in their forest districts. M. Edwards, M. Mac-
donald and G. Jones provided information on O. uncinata
in Scotland. A. Rigling provided information on growth,
biology and distribution of P. sylvestris. B. Wermelinger,
A. Frei and T. Lachat informed about xylophagous bee-
tles attacking P. sylvestris. A. Jacobs provided a photo of
a female of O. uncinata. A. Fateryga translated Russian
text passages. The Wildbienen-Kataster Baden-Wurttem-
berg, the EIS Leiden, the Bayerisches Landesamt fiir Um-
welt/Artenschutzkartierung Bayern, the Centre Suisse de
Cartographie de la Faune (CSCF), the Swiss Federal In-
stitute for Forest, Snow and Landscape Research (WSL),
the ZOBODAT database of the Biologiezentrum Linz, the
Database of Estonian zoological collections and the Glob-
al Biodiversity Information Facility database (GBIF Oc-
currence Download https://doi.org/10.15468/dl.6pw9im,
24.3.2020) provided distributional data. Molly Rightmy-
er and Christophe Praz reviewed the manuscript.

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Supplementary material |

List of distributional data of Osmia uncinata

Authors: Rainer Prosi, Andreas Miller

Data type: XLS file

Copyright notice: This dataset is made available under
the Open Database License (http://opendatacommons.
org/licenses/odbl/1.0/). The Open Database License
(ODbL) is a license agreement intended to allow us-
ers to freely share, modify, and use this Dataset while
maintaining this same freedom for others, provided
that the original source and author(s) are credited.

Link: https://do1.org/10.3897/alpento.4.53489 suppl 1

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